SUMMARY

All vertebrates regulate body temperature within narrow limits, regardless
of their physiological capabilities. When do these limits develop, and can
they be modified by manipulations of the developmental thermal environment? We
addressed these questions by incubating the eggs of the Madagascar ground
gecko, Paroedura pictus, at three temperatures and by assessing
thermoregulatory behavior in hatchlings. Thermoregulatory behavior was
assessed using a two-choice shuttle paradigm, and skin temperatures were
measured non-invasively using infrared thermography. The shuttling behavior of
hatchlings was systematically affected by the temperature at which they were
incubated, and follow-up tests suggested that this effect persisted for at
least three weeks post-hatching. The body temperature data from the shuttling
experiment were used to model thermoregulatory behavior in a complex thermal
environment; the model predicted systematic effects of incubation temperature
on thermal preference. The specificity of the alteration in thermoregulatory
behavior by incubation temperature is compelling and provides evidence for
powerful pre-hatching influences on a fundamental, life-sustaining behavioral
process.

Introduction

Animals inhabit and thrive in an extraordinary range of terrestrial and
aquatic thermal environments; from Arctic polar bears and Antarctic fish to
the many organisms that have adapted to life around superheated deep-ocean
thermal vents (Blumberg, 2002).
The adaptation of species to such a diversity of thermal environments has
required the alteration and coordination of many enzymatic systems. Yet, other
processes that contribute to these remarkable adaptations have essentially
been ignored. The possible contribution of developmental processes to the
setting of thermal regulatory ranges is one such example. Therefore, in the
present experiment, we manipulate the thermal environment of an egg-laying
reptilian species during incubation and assess the thermoregulatory behavior
of hatchlings. We show that incubation temperature plays a significant role in
shaping the thermoregulatory behavior of hatchlings.

The use of behavior to maintain thermal homeostasis is a vital
thermoregulatory component in all animals, regardless of their physiological
capabilities (Satinoff, 1978).
Many reptiles, including lizards, regularly shuttle between sun and shade (or
other warm and cool microenvironments) as a means of regulating body
temperature within a relatively narrow range
(Heath, 1970). The body
temperatures that trigger heat-seeking and heat-avoiding behaviors form lower
and upper thresholds that define the range of body temperatures within which
these ectotherms can tend to their non-thermoregulatory needs
(Barber and Crawford, 1977).
Interestingly, the factors that establish these thresholds have yet to be
identified.

Temperature is a critically important factor during development
(Satinoff, 1991). In reptiles,
eggs must be incubated within a narrow range of temperatures (approx.
10°C) to remain viable (Deeming and
Ferguson, 1991a). Within this range of viability, however, it is
known that the thermal environment modulates a variety of anatomical,
physiological and behavioral characteristics, including sex, growth rate,
size, pigmentation, anti-predator behavior and running speed
(Burger, 1998a;
Crews et al., 1998;
Deeming and Ferguson, 1991a;
Gutzke and Crews, 1988) Only
three studies, however, have examined the influence of incubation temperature
on thermoregulatory behavior in young reptiles
(Lang, 1987;
O'Steen, 1998;
Rhen and Lang, 1999a), and
only one of these examined the behavior of hatchlings. In the study of Lang
(1987), Siamese crocodile
(Crocodylus siamensis) eggs from a single clutch were incubated
either at 32.5-33.5°C or at 27.5-28°C, and subjects were then raised
on thermal gradients. (A thermal gradient is a surface that is heated at one
end and cooled at the other, thus establishing a continuous distribution of
temperatures.) Because crocodiles exhibit temperature-dependent sex
determination (TSD), only males were produced at the high incubation
temperature and only females were produced at the low incubation temperature.
Of the hatchlings, Lang assessed the thermal preference of four males and two
females on the thermal gradients. His results suggested that the hatchlings
incubated at the high temperature (i.e. males) preferred warmer temperatures
than the hatchlings incubated at the low temperature (i.e. females). Moreover,
this apparent difference in thermal preference persisted through at least 60
days post-hatching.

Although Lang's results are intriguing, the use of a small number of
subjects from a single clutch of eggs of a TSD species presents obvious
interpretational difficulties. Nonetheless, despite the methodological
problems with Lang's experiment, Deeming and Ferguson
(1991b) remarked that his
experiment “may indicate that differences in preferred body temperatures
between individuals, and between species... are not solely genetic traits but
may be physiologically acquired traits established during incubation... These
experiments need repeating on a larger scale with a full range of incubation
temperatures, including those that produce both males and females” (pp.
162-163).

The present experiment is in part a response to Deeming and Ferguson's call
for a more thorough and systematic investigation of the effect of incubation
temperature on the establishment of thermal regulatory ranges. The initial
step was to identify a reptilian species that satisfied a number of criteria
that allow us to avoid the methodological shortcomings of Lang's experiment.
Based on these criteria, we chose the Madagascar ground gecko (Paroedura
pictus), a nocturnal species that exhibits genetic sex determination
(GSD; L. Talent and B. E. Viets, unpublished data). P. pictus is, as
its name suggests, a ground-dwelling species that inhabits the dry forests,
savannas and semi-desert areas of southern Madagascar
(Henkel and Schmidt, 1995).
Moreover, it breeds easily and rapidly in captivity, with females producing a
clutch of two eggs every 3-4 weeks. Importantly, the embryo tolerates a wide
range of incubation temperatures (22-32°C). In addition, because
hatchlings weigh less than 1 g and, consequently, have little thermal inertia,
infrared thermography (IR thermography) can be used to measure dorsal skin
temperature noninvasively and thereby provide a reliable estimate of core body
temperature.

Materials and methods

Subjects

Adult Madagascar ground geckos (Paroedura pictus) (L.) were
obtained from a commercial breeder (Glades Herp, Inc., Fort Myers, FL, USA),
and a breeding colony of 10 females and five males was established. A pair of
females and a male were housed in an approximately 381 aquarium equipped with
a source of heat and hide boxes. Each aquarium was checked twice daily for the
presence of eggs. Once laid, each egg was transferred to an incubator inside a
small plastic container filled with moistened vermiculite; eggs were misted
with water three times a week to maintain adequate humidity. If multiple eggs
were found in the same aquarium, they were always placed in different
incubators. The adult geckos were fed crickets, coated with a calcium and
vitamin D dietary supplement, three times a week, and water was available
ad libitum. Geckos were maintained on a 12 h: 12 h L:D cycle (lights
on at 06.00 h).

Procedure

Once laid, each egg was transferred to one of three incubators at
temperatures of 22-24°C (hereafter designated as 23°C), 26°C or
30°C. The eggs remained in the incubators undisturbed until hatching. Of
the 67 hatchlings for which data are reported here, 78% were tested on the
night after hatching, 13% on the second night, and 9% on the third night
(subjects not tested on the first night post-hatching were distributed evenly
across conditions). Hatchlings remained in the incubator until testing and
were not fed until after the first test was completed.

The test began by placing the hatchling on the shuttle apparatus at 18.00
h. This apparatus consisted of a ceramic surface, comprised of Peltier diodes,
enclosed by a Plexiglas cylinder (radius=6 cm); the temperature of each 4 cm×
4 cm Peltier diode was manipulated using a custom-designed
computerized system that allows for accurate and stable delivery of current.
The temperature of one half of the surface within the cylinder was maintained
at 41°C, while the temperature of the other half was maintained at
16°C. These temperatures are above and below the range of body
temperatures tolerated by other nocturnal lizards and are similar to those
used in other shuttle experiments (Hammel
et al., 1967; Templeton,
1970).

The IR thermography system consists of a thermoelectrically cooled scanner,
computer interface hardware, and acquisition and analysis software (FLIR
Systems, Portland, OR, USA). To accurately measure absolute skin and diode
temperatures using IR thermography, it was first necessary to measure the
emissivity of the skin. (Emissivity is the ratio of the radiant energy emitted
by a surface to the energy emitted at the same temperature by a black body
radiator.) To accomplish this, the skin of hatchlings was heated to at least
40°C, and an emissivity value was obtained. Across a range of skin
temperatures, values acquired using IR thermography were compared with those
acquired using a reference thermocouple attached to the skin. Finally, average
emissivity values were obtained and a regression equation was derived with the
thermocouple temperature as the independent variable and the IR temperature as
the dependent variable. The equation was then used to adjust the dorsal skin
temperature values obtained using IR thermography. The same process was used
for measurement of diode surface temperature.

Finally, the IR system was programmed to record an image to disk every five
seconds beginning at 21.00 h and ending 6 h later at 03.00 h; thus, data were
recorded exactly midway through the lights-off period. The following morning,
the animal was removed from the apparatus, weighed, and body length (from tip
of snout to tip of tail) was measured.

Data analysis

Data were analyzed for each run by reviewing all 4320 images and
determining when crossovers occurred. A `crossover' was defined as the
movement of three-quarters of the subject's body (defined as the region from
the snout to pelvic girdle) across the dividing line between the hot and cold
regions within a 30-s period. (The use of a very conservative definition of
crossover excluded many crossing events but was necessary to standardize the
measurement procedure across subjects and experimental conditions.) The time
of a `cold exit' was defined as the last image in which the hatchling was
located on the cold side of the apparatus before a crossover began, and the
time of a `hot exit' was defined as the last image in which the hatchling was
located on the hot side of the apparatus before a crossover began
(Fig. 1). Then, using the data
analysis functions of the IR system, the temperature in the mid-back region of
a hatchling was measured for each cold and hot exit. The mean and standard
deviation of these values were calculated for each subject and used for
subsequent analyses. For each subject, mean exit temperatures were excluded
from the analyses when they were derived from fewer than eight crossovers;
eight hot exit temperatures and five cold exit temperatures, evenly
distributed across experimental conditions, were excluded for this reason. In
addition, for each incubation temperature, individual values that exceeded the
mean ± 1.96 S.D. were excluded as statistical outliers; for the
analysis of first-night data, only two cold-exit data points and three
hot-exit data points were excluded as outliers.

Infrared thermographs of a newly hatched Madagascar ground gecko
Paroedura pictus exhibiting shuttling behavior. The subject is
confined to a Plexiglas cylinder and chooses between a surface temperature of
16°C on the left (blue surface) and 41°C on the right (yellow
surface). In this 2-min sequence, the hatchling begins on the cold side of the
apparatus (A). In the next frame (B), it has crossed over to the hot side
where it remains stationary and gains heat from the hot floor (C). Eventually,
it begins to move again (D) and crosses back over to the cold side of the
apparatus (E) where it gradually loses heat to the cold surface (F). As
indicated, the labels `cold exit' and `hot exit' denote the frames preceding a
crossover to the hot and cold side of the apparatus, respectively.

In order to extrapolate from the two-choice shuttle data to the behavior of
hatchlings in a more complex thermal environment, a dual-limit stochastic
model (Barber and Crawford,
1977) was implemented using Mathematica (Version 4.0, Wolfram
Research, Inc., Champaign, IL, USA). This model assumes the presence of upper
and lower threshold detectors with stochastic response characteristics defined
by a mean and standard deviation and also uses these response characteristics
to predict how an animal would behave in an environment where many thermal
choices are available (e.g. a thermal gradient). Thus, this model can provide
an estimate of an animal's `thermal preference'
(Fraenkel and Gunn, 1961).

Results

As expected, incubation temperature had a profound impact on the growth and
development of the geckos (Fig.
2). With increasing incubation temperature, incubation time
decreased substantially (F2,64=265.4,
P<0.0001). In addition, both body length
(F2,64=8.0, P<0.001) and body mass
(F2,64=6.9, P<0.002) increased as incubation
temperature increased. It is clear from the proportional changes in incubation
time and hatchling body length and body mass that the growth rate of the
embryos was accelerated at the higher incubation temperatures, which is
consistent with previous research on other reptiles
(Deeming and Ferguson, 1991a).
Thus, these results confirm the efficacy of the independent variable,
incubation temperature, in modulating at least some basic developmental
processes in our subjects.

The effect of incubation temperature on (A) incubation time, (B) body
length and (C) body mass of newly hatched Madagascar ground geckos
Paroedura pictus. Body length and body mass were measured within two
days of hatching. For all measurements, the number of subjects per group was
20 (at 23°C), 23 (at 26°C) and 24 (at 30°C).
*Significant difference between adjacent points.
†Significantly different from the other two points.

Although incubation temperature did not have a significant effect on hot
exit temperature (F2,53=1.4), its effect on cold exit
temperature was highly significant (F2,57=8.7,
P<0.001; Fig. 3).
Post-hoc analyses revealed that each step-wise increase in incubation
temperature resulted in a significant increase in cold exit temperature
(P<0.05), from an average of 23.9±0.3°C at the lowest
incubation temperature to an average of 25.6±0.3°C at the highest
incubation temperature. These differences in thermoregulatory behavior cannot
be accounted for by differences in overall activity, as there were no
significant differences between groups in the number of crossovers performed
during the 6 h tests (cold exit: F2,64=1.2; hot exit:
F2,64=1.2).

The effect of incubation temperature on dorsal skin temperatures of newly
hatched Madagascar ground geckos immediately prior to crossovers to the (A)
cold (hot exit) and (B) hot (cold exit) sides of the apparatus. For cold exit
temperatures, the number of subjects per group was 17 (at 23°C), 22 (at
26°C) and 21 (at 30°C); the respective numbers for hot exit
temperatures were 15, 21, and 20. *Significant difference between
adjacent points.

Of the five breeding trios of two females and one male, four trios each
contributed 10-12 eggs to the study and one trio contributed 22 eggs. For this
last trio alone, incubation temperature had a significant effect on cold exit
temperature (F2,18=6.8, P<0.01), with cold
exit temperature increasing from an average of 24.1±0.5°C at the
lowest incubation temperature to an average of 26.5±0.6°C at the
highest incubation temperature. Despite the relatively small number of
subjects in the other trios, incubation temperature had a statistically
significant effect on cold exit temperature for one of them
(F2,8=14.2, P<0.005), with cold exit
temperature increasing from an average of 22.9±0.3°C at the lowest
incubation temperature to an average of 26.0±0.5°C at the highest
incubation temperature.

It is possible that body size or body length, both of which increased with
increasing incubation temperature (see Fig.
2), mediated the effects of incubation temperature on our measures
of thermoregulatory behavior. There was, however, no effect of these body size
measures on cold exit temperatures. Specifically, neither body length
(r2=0.02, N=56) nor body weight
(r2=0.03, N=60) accounted for significant
proportions of the variance in cold exit temperature.

To examine the stability of the effect of incubation temperature on
thermoregulatory behavior, a subset of hatchlings from each condition was
tested twice more, at 7-15 and 14-24 days post-hatching. These subjects were
housed in aquaria similar to those used to house the adults. Most importantly,
the aquaria were heated at one end, thus allowing hatchlings to thermoregulate
behaviorally throughout the day and night between tests. Although the number
of subjects tested more than once in the 23°C (N=5), 26°C
(N=7) and 30°C (N=7) conditions is small (in part owing
to mortality), the pattern observed in these follow-up tests is similar to
that seen in Fig. 3.
Specifically, for this subset of subjects incubated at 23°C and 30°C,
mean cold exit temperatures were, respectively, 24.1±0.5°C and
24.8±0.7°C on the first test night, 24.1±0.3°C and
25.0±0.4°C on the second test night, and 23.8±0.5°C and
25.3±1.2°C on the third test night. The consistency of this finding
is particularly surprising given the extended acclimation period outside of
the incubator and the lack of experimental control over the time when feeding
last occurred (Lang, 1987).
Thus, these data provide preliminary but suggestive evidence that the
differences in thermoregulatory behavior induced by differences in incubation
temperature remain stable beyond the first few days post-hatching.

The shuttling behavior of lizards has been modeled as comprising upper and
lower thresholds that govern the timing of crossovers during shuttling
behavior (Barber and Crawford,
1977). In addition, these thresholds are stochastic rather than
absolute, exhibiting normal frequency distributions with characteristic means
and standard deviations. When these threshold distributions are sufficiently
non-overlapping and the body temperature of the lizard lies between the two
thresholds, the model predicts that the lizard's behavior will be largely
non-thermoregulatory, thus freeing the animal to engage in other behaviors.
The shuttle apparatus compels a choice between hot and cold temperatures
(unless the animal straddles the two temperature zones, as occasionally
happens), thereby forcing the body temperature of the subject beyond each
threshold and allowing the experimenter to collect statistically meaningful
threshold temperature data.

To justify the assumption of normality, the six frequency distributions
(cold exit and hot exit distributions at each of the three incubation
temperatures) were tested using the Kolmogorov—Smirnov normality test.
Although one of the six distributions deviated significantly from normality
(hot exit, 23°C: χ2=10.5, d.f.=2, N=641,
P=0.01), the remaining five distributions did not
(1.2<χ2<5.6, d.f.=2, 410<N<736,
P>0.10).

Thus, from the present data, the means and standard deviations of cold and
hot exit temperatures were entered into the stochastic model. First, as
expected, the frequency distributions of the cold exit temperatures exhibit an
orderly progression with increasing incubation temperature
(Fig. 4A); the hot exit
temperatures also exhibit an orderly progression although, as described above,
this effect was not significant. Next, the model uses the threshold
information provided by the two-choice temperature selection experiment
employed here to predict the behavior of animals on a continuous thermal
gradient. Specifically, as shown in Fig.
4B, the curves for `heating transitions' indicate the probability
that a hatchling with a specific dorsal skin temperature will move toward a
hotter region of the environment; similarly, the curves for `cooling
transitions' indicate the probability that a hatchling with a specific dorsal
skin temperature will move toward a cooler region of the environment. These
two curves intersect at the point where a hatchling is equally likely to move
toward hot or cold. As shown in the insert in
Fig. 4, this point of
intersection, which can be conceptualized as the `temperature preferendum',
increases systematically with incubation temperature.

(A) Frequency distributions of dorsal skin temperatures for cold and hot
exit temperatures based on the means and standard deviations averaged across
hatchlings. Distributions are presented separately for hatchlings incubated at
23°C (blue), 26°C (green) and 30°C (red). (B) Transition
probabilities calculated using the dual-limit stochastic model of Barber and
Crawford (1977). The heating
transition curves (solid lines) indicate the probability that a hatchling,
behaving in a complex thermal environment, would move toward heat; the cooling
transition curves (broken lines) indicate the probability that a hatchling
would move away from heat. The point of intersection of the two curves
indicates an equal likelihood of moving toward or away from heat. As shown
most clearly in the insert, the dorsal skin temperature at which this
equilibrium point occurs increases systematically with incubation
temperature.

Discussion

The aim of this experiment was to investigate the influence of incubation
temperature on post-hatching thermoregulatory behavior using a reptilian
species that breeds easily in captivity and that could be readily tested using
our experimental procedure. The results clearly and reliably demonstrate for
the first time in a GSD reptile a direct effect of incubation temperature on
thermoregulatory behavior that is present at hatching and that may persist
through at least the first three weeks post-hatching. The use of a GSD species
is particularly significant because, with only a few exceptions, investigators
have focused on epigenetic processes in reptilian species that exhibit TSD; in
turn, this focus has fostered the view that epigenetic processes are perhaps
most salient in TSD species. In contrast, incubation temperature has been
shown to influence a variety of post-hatching behaviors in the pine snake
(Pituophis melanoleucus), a GSD species (Burger,
1998a,
b;
Burger and Zappalorti, 1988).
Thus, the present results provide additional support for considering the
importance of the developmental thermal environment in GSD reptiles and open
up a wide range of important questions concerning the development and
evolution of homeostatic systems in a variety of vertebrate species.

There are several methodological features of this experiment that deserve
some comment. First, by testing hatchlings, it was expected that the
assessment of cold and hot exit temperatures would be relatively
uncontaminated by possible effects of posthatching thermal acclimation and
other possible influences of the rearing environment. This is not to say,
however, that this focus on hatchlings could not have introduced other issues
that may have a bearing on the present results, including the differential
effects of incubation temperature on the size and hormonal composition of the
yolk (Deeming and Ferguson,
1989; Rhen and Lang,
1999b).

Second, the use of IR thermography was significant for providing an
accurate measure of thermoregulatory behavior and its consequences without the
need to use probes that can interfere with behavioral expression. Although
direct and simultaneous measures of core temperatures would perhaps have been
ideal, we chose a species that is particularly small at hatching to minimize
differences between core and skin temperatures. Specifically, given their
small size (<1 g) and low thermal inertia, it is reasonable to assume that
our IR measurements provided reliable estimates of core body temperature, even
during rapid changes in temperature. This assumption was borne out by
measuring changes in cloacal temperature (using a thermocouple) and skin
temperature (using IR thermography) in a dead hatchling during a series of
cooling tests. As expected, IR thermography recorded changes in dorsal skin
temperature that were at least as rapid as those recorded using the
thermocouple.

Given that P. pictus is classified as a nocturnal species, one
might wonder whether the two thermal choices used in the shuttle apparatus
(i.e. 16°C and 41°C) were appropriate. First, our subjects exhibited
systematic shuttling between the two sides of the apparatus and rarely
indicated through their behavior that the two surfaces were either too hot or
too cold. Second, although we have no information on the natural thermal
microenvironment of P. pictus, the body temperatures of geckos in
general, and at least two nocturnal reptiles (the night lizard Klauberina
riversiana and the shovel-nosed snake Chionactis occipitalis),
range from the mid-teens to the mid-thirties
(Brattstrom, 1965). Finally, it
should be stressed that the classification of a reptile as nocturnal can
foster the mistaken impression that thermoregulatory shuttling is a less
important feature of its daily activity. Indeed, some geckos and lizards that
have been classified as nocturnal have nonetheless been observed basking in
direct sunlight (Brattstrom,
1965; Templeton,
1970).

We chose to model the behavior of hatchlings to predict thermal gradient
behavior rather than simply measure thermal gradient behavior directly. We
made this choice because the behavior of a reptile on a thermal gradient is
shaped by its upper and lower thresholds and that, between these thresholds,
behavior is highly variable and probabilistic. As a result, many days of
observation are required to gather reliable data using a thermal gradient
(Barber and Crawford, 1977).
This requirement did not seem practical given (1) the age and fragility of our
subjects and (2) that the primary goal in this experiment was to define the
characteristics of the upper and lower thresholds of our subjects, a goal that
is best accomplished using a shuttle paradigm.

The mechanism by which incubation temperature influences post-hatching
thermoregulatory behavior is unknown. Incubation temperatures could influence
the course of thermoregulatory development through a process of `thermal
imprinting'. Such imprinting may be irreversible, even after acclimation to
different environments (Winkler,
1985). In addition, because shuttling behavior in lizards is
modulated by a combination of brain, core and skin temperatures
(Hammel et al., 1967),
incubation temperature may exert its effects by altering the development of
thermosensitive neurons. It is equally plausible, however, that incubation
effects are mediated by differences in metabolic rate or a related variable
(O'Steen and Janzen, 1999). A
better understanding of the mechanisms that underlie this phenomenon will be
one necessary step in understanding the ecological significance of variations
in incubation temperature.

There have been remarkably few studies concerning the role of epigenetic
processes in the development of homeostatic regulatory ranges, including those
concerned with temperature regulation. For example, there is intriguing
evidence that cultivation temperature shapes thermoregulatory behavior in the
nematode Caenorhabditis elegans
(Hedgecock and Russell, 1975;
Mori and Ohshima, 1995), and
that the developmental thermal environment irreversibly modifies
thermoregulatory behavior in fish
(Winkler, 1985). These
findings on the development of thermoregulatory behavior in worms, fish and
reptiles might prove to be of broader significance for the development of
thermoregulatory processes in birds and mammals, including humans. Although
one might suppose that genetic influences on thermoregulatory development
would be paramount in homeothermic avian and mammalian species, there is
little empirical basis for such a supposition. Indeed, it appears that
incubation temperature can modify some aspects of post-hatching
thermoregulation in an endotherm, the Muscovy duck Cairina moschata
(Nichelmann and Tzschentke,
1997). Finally, it should also be stressed that such developmental
effects are not likely to be restricted to the thermal domain; the regulatory
ranges of other homeostatic systems may also be established early in
development (Blumberg,
2001).

ACKNOWLEDGEMENTS

This work was supported by a Faculty Scholar Award from the University of
Iowa to M.S.B. Preparation of this manuscript was supported by grants from the
National Institute of Mental Health (MH50701) and the National Institute of
Child Health and Human Development (HD38708). We thank Lloyd Frei and Keith
Miller of the Judson S. Brown Instrumentation Shop in the Department of
Psychology at The University of Iowa for their critical contributions to the
design and construction of the diode apparatus and its accompanying control
system. We also thank Elliott Blass, David Crews and Evelyn Satinoff for their
many helpful comments on an earlier draft of the manuscript, and Tricia Knoot
for technical assistance.

Winkler, P. (1985). Persistent differences in
thermal tolerance among acclimation groups of a warm spring population of
Gambusia affinis determined under field and laboratory conditions.
Copeia2,456
-461.

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